Friday, March 8, 2013

The Magic of Metamorphosis

by Heather Price

photo courtesy of: the Butterfly site

Many
of us can remember catching tadpoles as children and watching,
captivated, as they slowly but surely sprouted legs and developed into
frogs. Others may recall watching a chrysalis form for the first time,
and wondering at the mysterious inner-workings of that dark
cocoon, which allowed a creeping caterpillar to transform into a magnificent,
winged butterfly.As
adults, we have hopefully not lost the ability to marvel at
the incredible process of metamorphosis. What many may not realize, however, is that radical transformations such as
the tadpole and caterpillar undergo, are actually quite common throughout the animal kingdom. The vast majority of insects (not only butterflies!) start out life as larvae before turning into their adult form, and in the marine world, this type of life cycle is the modus operandi.

photo courtesy of: National Geographic

The ocean is home to an incredible diversity of invertebrates (meaning animals that don't have a backbone), which all begin their lives as tiny, drifting plankton before metamorphosing into their adult form. Many familiar tidepool species (such as the ochre sea stars pictured at right), fall into this category.
Sea stars actually go through multiple larval stages before becoming an adult with five (or more) arms. An embryo will first develop into a bipinnaria larva, then a brachiolaria larva, before eventually becoming a juvenile five-armed sea star. For a great visual of this process, see the video below:

Animation of sea star development, showing multiple larval stages.

courtesy of: Daniel Brown

Having a
complex, multi-stage life-cycle, like that of the sea star, may seem like more trouble than its
worth to us direct developers, but there are many benefits to metamorphosis which can outweigh the costs. Most
marine larvae hatch from eggs which are broadcast in large numbers into
the water column. The larvae then join the ranks of zooplankton
drifting at the whim of the currents. As plankton, they do not compete
with the adults of their species for space or food, and they also may
drift a long ways before settling down, thus decreasing the risk of both
inbreeding and local extinction. These and other benefits help explain why so many species have a larval stage, especially in the marine environment, but the mechanisms underlying how metamorphosis occurs are where things start to really get interesting!Whether
it be a frog or a butterfly on land, or a mussel or jelly in the sea, all
metamorphosis is hormonally controlled. The signaling pathways
that lead to metamorphosis in insects and amphibians are well-studied, and better understood than those of most marine species. Tadpole metamorphosis is controlled by hormone signaling
via the HPT axis. External stimuli (such as temperature, light, or water level) first trigger receptors to send a message to the
hypothalamus, causing it to secrete corticotrophin
releasing factor (CRF), which then stimulates the pituitary gland to
secrete thyroid stimulating hormone (TSH), which causes the thyroid to
release two forms of thyroxine, or thyroid hormone (T4 and T3). Thyroxine is then responsible for triggering growth of new body parts, and breaking down those in the larval form that are no longer needed.

Tata, 2006.

Thyroxine is also involved in the inducement of metamorphosis in many marine species, though the specifics of their hormonal cascades are not as well understood. Much is known about what happens anatomically in many species during metamorphosis, however. One fascinating example is a small marine animal which is often mistaken for algae, (if not completely overlooked).

Bugula neritina is a sessile (non-moving), colonial invertebrate that belongs to the Phylum Bryozoa. It is native to the Mediterranean, but has now spread world-wide, and can often be seen in purple or brown clumps on piers or boats in local bays. Bugula have ciliated, non-feeding larvae which are released from a brood chamber, before swimming in the water column for anywhere from a few hours to several days, depending on how quickly they encounter a suitable place to spend the rest of their lives.

Bugula sp. larvae photo courtesy of: angelfire.com

Bugula neritina adult colonyphoto courtesy of: reefedu.com

When Bugula larvae want to check out potential real estate, they use a structure called the vibratile plume, (which consists of long, feather-like cilia), to feel out a substrate. Tactile sensing is thought to play a large role in this surveying behavior, but recent studies have also shown that the vibratile plume contains adregenic receptors (those that bind adrenaline and noradrenaline), suggesting that hormones are involved in this process as well. Once the larvae choose a particular spot, they attach themselves to the surface with a mucus-like substance, and then rapidly begin the process of transformation. The attached larva will reorient itself so that the vibratile plume is sticking out on top, and then a drastic eversion of the internal sac (which comprises most of the body volume) will occur. Most of the larval structures will be then adsorbed and completely new adult structures will form in their place. Within 48 hrs, multiple zooids with feeding cilia and complete digestive tracts will be formed, and the adult animal will be fully established. This colony of zooids can then become reproductive (and begin the cycle again) within just eight days after settlement! The molecular mechanism underlying metamorphosis in this species was recently investigated by Wong et al., and they found drastic increases in expression of proteins involved with energy metabolism and protein synthesis during metamorphosis (not surprisingly), as well as upregulation of proteins specific to the Wnt signaling pathway. This pathway is well-studied in many organisms, and appears to be implicated in Bugula metamorphosis as well. (For more detailed information on this, see the article by Wong et al. listed in the references!) Based on the patterns of gene expression seen in this study, it seems that many larval structures are already pre-programmed to turn into specific adult structures.

Bugula neritina metamorphosis Wong, et al., 2012

At first glance, Bugula neritina may appear to be nothing more than a sedentary brown clump, but closer investigation of this species has revealed a fascinating and complex life cycle involving dramatic transformation. Current research is beginning to elucidate the underlying magic of metamorphosis in a plethora of species, and these findings will hopefully force us to stop and wonder anew at the amazing process of transformation happening all around us.

As an aside:

“I cannot make you understand. I cannot make anyone understand what is happening inside me. I cannot even explain it to myself.”
-Franz Kafka, The MetamorphosisHopefully, you have not come away from this blog feeling like poor Gregor in Kafka's famous short story! (Hopefully, you also have not just recently awoken to find yourself a large beetle...) I imagine some caterpillars and brachiolaria larvae may be able to empathize with Gregor, however.ReferencesLynch, William. 1947. The behavior and metamorphosis of the larva of Bugula Neritina . The Biological Bulletin 92:115-150.Oguro, C., M. Komatsu, and Y. Kano. 1976. Development and Metamorphosis of the sea-star, Astropecten scoparius valenciennes. Biological Bulletin 151: 560-573. Pechenik,
J. 1999. On the advantages and disadvantages of larval stages in
benthic marine invertebrate life cycles. Marine Ecology Press
177:269-297.

Tata, J. 2006. Amphibian metamorphosis as a model for the developmental actions of thyroid hormone. Molecular and Cellular Endocrinology 246:10-20.